Winter ranges have been identified for most neotropical migrant
bird species, those that spend the winter months in Central and South
America and summer months in North America. Published accounts and
specimen collections of the Northern Black Swift (Cypseloides niger
borealis) during spring and fall migration are extremely limited and
winter records are nonexistent. We placed light-level geolocators on
four Black Swifts in August 2009, and retrieved three a year later. Data
from the geolocators revealed initiation of fall migration (10 to 19 Sep
2009), arrival dates at wintering areas (28 Sep to 12 Oct 2009),
departure dates from wintering areas (9 to 20 May 2010), and return
dates to breeding sites (23 May to 18 Jun 2010) for Northern Black
Swifts breeding in interior North America (Colorado, USA). Northern
Black Swifts traveled 6,901 km from the Box Canyon breeding site and
7,025 km from Fulton Resurgence Cave to the center of the wintering
area. The swifts traveled at an average speed of 341 km/day during the
2009 fall migration and an average speed of 393 km/day during the 2010
spring migration. This is the first evidence that western Brazil is the
wintering area for a subset of the Northern Black Swift, extending the
known winter distribution of this species to South America.

Geographic Scope: United Kingdom; United States Geographic Code: 4EUUK United Kingdom; 1USA United States

Accession Number:

285207235

Full Text:

Knowledge of patterns and timing of migration of the Northern Black
Swift (Cypseloides niger borealis) (Frontispiece) is virtually
non-existent and the species' winter range is unknown. Published
accounts and specimen collections for this subspecies during spring and
fall migration south of the United States exist only for sites in
south-central Mexico (Stiles and Negret 1994), off the Guatemalan coast
(Davidson 1934), and off the southwest coast of Chiapas, Mexico
(Buchanan and Fierstine 1964). Negret collected the first specimens of
Northern Black Swift for South America in southwestern Colombia in
October 1992 and 1993, suggesting a South American winter destination
(Stiles and Negret 1994). Fall specimens originally reported to be C. n.
costaricensis from south-central Mexico (Webster 1958) were subsequently
identified as C. n. borealis (Stiles and Negret 1994). Flocks of Black
Swifts thought to be migrating C. n. borealis in Costa Rica in spring
had no specimens collected for confirmation (Stiles and Skutch 1990).
Kiff (1975) tentatively assigned a female swift collected in Costa Rica
to C. n. borealis based on wing and tail measurements that are within
ranges for C. n. costaricensis, further highlighting the uncertainty of
migration and winter distribution for this subspecies. Winter records
for Northern Black Swift are non-existent.

Several factors contribute to the lack of knowledge about migration
and winter distribution of this species, including difficulty in
accurate field identification of individuals due to high and rapid
flight, problems differentiating this species from similar-size members
of Cypseloides that occupy Central and South America, and inability to
verify observation records. No band recoveries exist outside of the
United States from ~200 Northern Black Swifts banded from 1950 to
present (Bird Banding Laboratory, pers. comm.).

Currently, satellite tracking devices which provide accurate
tracking of individuals are not sufficiently small to place on a species
the size of Black Swifts. However, light-level geolocators, devices that
record ambient light levels at fixed intervals, are highly effective
instruments for tracking long-distance migratory species and are
sufficiently small to place on swifts. They are battery-powered
instruments with a microprocessor, clock, and memory for data storage;
geographical positions can be calculated from the data collected by the
devices.

Geolocators must be retrieved to download data, and the Black Swift
is particularly suited to recapture due to its high breeding colony
fidelity and an individual propensity to reuse the same nest from year
to year (Foerster 1987, Collins and Foerster 1995, Marin 1997, Hirschman
et al. 2007). We placed geolocators on four Northern Black Swifts with
the objective to gather information about the migratory path, timing,
and winter destination of this species.

Identifying the connectivity of a migrating species between
breeding sites and wintering areas is crucial to understanding the
species' ecology and in guiding conservation efforts. Time spent in
widely separated and ecologically disparate locations by migrating
species and the strength of this link can have great biological
consequences for individuals and populations, including reproductive
success, population dynamics, behavioral ecology, evolution, and
response to changing selective pressures (Webster et al. 2002). Advances
in geolocator technology can provide this information by tracking
individuals at high resolution. We conducted this study because
information on migration and wintering areas of Northern Black Swifts
was virtually non-existent (Lowther and Collins 2002, Wiggins 2004). The
small sample does not tell us how weak or strong the migratory
connectivity is for this subspecies, but forms a foundation for
additional knowledge of this species' ecology and can guide future
studies.

METHODS

Study Sites.--Northern Black Swifts nest at or near waterfalls
typically inaccessible due to steep and vertical configuration (Knorr
1961, Levad et al. 2008). More than 100 breeding sites of this species
have been documented in North America (Lowther and Collins 2002, Levad
et al. 2008) with only a few records of alternate types of sites such as
sea caves in California (Legg 1956), small cave-like boulder
configurations in streams (Foerster and Collins 1990, Johnson 1990,
Hurtado 2002), and caves (Davis 1964, Northern British Columbia Caving
Club 2003).

We chose Fulton Resurgence Cave (39[degrees] 49' N,
107[degrees] 24' W) and Ouray Box Canyon Falls (38[degrees] 1'
N, 107[degrees] 40' W) in Colorado because of accessibility and the
probability of capturing and recapturing Black Swifts using hand-held or
mist nets. These breeding colonies are two of the largest in Colorado
(Levad et al. 2008) with an average of eight nesting pairs (range 7-9, n
= 6 yrs) at Fulton Resurgence Cave (KMP, pers. obs.) and an average of
11 nesting pairs (range 715, n = 10 yrs) at Box Canyon Falls (Hirshman
et al. 2007, Levad et al. 2008). Fulton Resurgence Cave is a limestone
cave with a small stream issuing from it, forming a microhabitat
conducive for a Black Swift breeding colony (Knorr 1961). Mist nets
placed near the mouth of the cave, the only ingress/egress for swifts,
have resulted in a recapture rate of 41% since banding of adults began
in 2006 (KMP, pers. obs.). Box Canyon Falls is a popular tourist site
and walkways provide views of the falls. The walkways allow access to
several nest sites and, with the aid of ladders, several nests can be
reached with hand-held nets.

Data Collection.--We used four Mk10S model geolocators,
manufactured by the British Antarctic Survey (BAS), programmed to
continuously measure light levels every minute and archive the maximum
measurement for each 10-min period. The devices weighed 1.2 g, measured
18 x 9 x 6 mm, and have a light sensor mounted at the tip of a 10-mm
stalk angled at 15[degrees] to prevent it from being covered by
feathers. The instruments are encapsulated in a water-resistant housing
with two external terminals for commands and data transfers.

We designed a backpack harness system modified from Buehler et al.
(1995) because Black Swift legs are too attenuated for the leg-loop
harness often used for geolocators on passerines (Rappole and Tipton
1991). The harness material, 5 mm tubular Teflon ribbon (Bally Ribbon
Mills, Bally, PA, USA), was attached at four points to the geolocator
and crossed under the keel. We secured the free ends of the ribbon with
size 69 bonded right twist Kevlar thread (The Thread Exchange Inc.,
Weaverville, NC, USA) and stitched the ribbon where it crossed the keel
to avoid shifting. We applied cyanoacrylate glue on all stitches and cut
ends to prevent fraying.

We attached geolocators to four adult Black Swifts in August 2009,
three at Fulton Resurgence Cave (2 females, 1 male) and one at Box
Canyon Falls (male); the birds weighed 49.5-51.5 g. Each geolocator,
including harness materials, weighed 1.5 g, representing 2.9-3% of body
weight, well within guidelines suggested by Caccamise and Hedin (1985).

Data Analysis.--We conducted pre-deployment calibration for ~9 days
and post-deployment calibration for ~7 days by placing them at a known
location with a clear view of the sky. We retrieved three of the four
geolocators in July and August 2010.

We used software programs (BASTrak) developed by BAS to download,
process, and interpret data archived by the loggers, each of which had
collected data throughout their entire deployment. We rejected latitude
data gathered ~30 days before and after the equinoxes since day lengths
at the equinoxes are equal at all latitudes, resulting in poor location
fixes. Internal clocks maintained accuracy during deployment and there
was no need to correct for clock drift.

Two values are required for analyzing and plotting the geolocator
data: the dusk/dawn light transition threshold and the corresponding sun
elevation angle at this threshold. We chose a sensitive light transition
threshold value of two to reduce variation in day length due to the
effects of shading which influences the resulting distribution of
location fixes. We used static pre-deployment calibration to calculate
the corresponding sun elevation angles ( 6.4[degrees], 6.5[degrees], and
6.6[degrees]). We calculated times of sunrise and sunset using
TransEdit2; positions were calculated with BirdTracker which derives
longitude from absolute time of local midday/midnight and calculates
latitude by comparing day/night length, a technique which provides two
geographical positions/ day. We used only midnight fixes to produce maps
based on the assumption that swifts were roosting at night and migrated
during the day. We identified days with irregular shading events,
resulting in shorter day lengths or anomalous transition times, by
visually inspecting sunrise and sunset times and excluded them from the
analysis. An average of 145 fixes for each bird remained to map
wintering range and an average of 26 fixes remained to map the spring
migration path. Mapping of fall migration was not possible due to
overlap with the fall equinox.

We calculated kernel density surfaces using the wintering area data
from each geolocator with the Spatial Analyst Kernel Density function
(ESRI 2009). This function calculates density of fixes in a search
radius around those fixes. These densities fit a smoothly curved surface
over each location. The surface value was highest at the location of the
point and diminished with increasing distance from the point. We used a
fixed kernel with a search radius of 185 km to compensate for the
approximate average error in latitude and longitude known to occur in
geolocator data (Phillips et al. 2004). The kernel function is based on
the quadratic kernel function described in Silverman (1986). We
calculated the density surfaces at 1-km resolution as this is adequate
to capture density at a small scale over a large geographic area. We
calculated 90%, 75%, and 50% density polygons from the kernel density
surfaces to enhance graphic displays of higher use density areas. We
used the average nearest-neighbor distance function in ArcInfo Spatial
Statistics (ESRI 2009) to characterize the spatial point pattern of
winter locations. This function quantifies and characterizes the spatial
pattern of each geolocator and indicates if the pattern is evenly
dispersed, random, or clustered compared to a spatial random
distribution. We estimated approximate migration duration, arrival, and
departure events from plotting longitude and date. We used the 50%
kernel density polygons for all three swifts to describe land cover use
and overlaid those with a global land cover layer using 2009 satellite
imagery at a 300-m resolution produced by the European Space Agency
GlobCover 2009 Project (Bontemps et al. 2010).

RESULTS

Geolocators recovered from two females at Fulton Resurgence Cave
and one male at Box Canyon Falls represent a 75% recovery rate. The
Black Swifts initiated fall migration from Colorado beginning on l0
September and continued through 19 September 2009. We used longitudinal
information around the time of the autumnal equinox and documented the
swifts arrived at their wintering location in South America between 28
September and 12 October 2009. Approximate dates of migration initiation
north from wintering areas began on 9 May and continued through 20 May
2010. Dates of arrival at breeding sites began 23 May and continued
through 18 June 2010 (Table 1, Fig. 1).

Kernel density estimates indicate all three birds over-wintered
primarily in the lowland rainforest of western Brazil with some kernels
extending into Bolivia, Colombia, Peru, and Venezuela (Fig. 2). Average
nearest-neighbor distance analysis for all geolocators exhibited
clustering with nearest-neighbor ratios = 0.89 (P = 0.02), 0.74 (P <
0.001), and 0.77 (P < 0.001) for geolocator #553, #554, and #556,
respectively. The distance between the Ouray Box Canyon Falls breeding
site and the center of the wintering range in Brazil (#554) is 6,901 km
and the average distance between the Fulton Resurgence Cave breeding
site and the center of the wintering range in Brazil (#553 and #556) is
7,025 km. The swifts traveled at an average speed of 341 km/day during
the 2009 fall migration and an average speed of 393 km/day during the
2010 spring migration. The inaccuracy of geolocators precludes precise
calculation of an average daily distance covered by each bird.

The land cover overlay maps for 50% kernel density areas for all
three birds indicate a dominant land cover (>86%) of closed to open
broadleaved evergreen or semi-deciduous forest and a small percentage
(2-10%) of the kernel density areas are classified as closed to open
broadleaved forest regularly flooded. Areas of mosaic
cropland/vegetation, mosaic forest shrubland/grassland, closed to open
shrubland or grassland, bare areas, and water bodies represented <2%
use.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

DISCUSSION

We documented the timing of fall and spring migration, wintering
area, and spring migration paths for three Northern Black Swifts using
geolocators. The return dates to breeding sites after spring migration
and dates of the initiation of fall migration correlate with data
collected in other research (Hirschman et al. 2007). Wintering area
locations were previously unknown, and only sporadic reports existed
which did not fully delineate migratory paths.

The highest kernel density estimates indicate the three birds
wintered almost entirely within the State of Amazonas, Brazil. The
clustering of the three individuals exhibited by nearest-neighbor
analysis might be expected based on the birds seeking a physiologically
optimal climate, preferred habitat, abundant prey, or other factors
within a certain geographic area. Amazonas is composed almost entirely
(~98%) of lowland rainforest at elevations between 34 and 116 m. The
area is sparsely populated with a density of 2.05 inhabitants/[km.sup.2]
with 78% of the population in cities (IBGE 2011). Amazonas has an
equatorial tropical rainforest climate with annual rainfall of 1.50-2.50
m and all months have a mean precipitation of at least 60 mm (IBGE
2011). The average temperature per day per year is 26.7[degrees]C
(23.3-31.4[degrees]C) with high humidity (Brasil Travel Guide 2011).

The three birds tracked in this study represent only a small
geographical subset of the Northern Black Swift population and further
studies are needed to delineate more completely the full extent of the
wintering distribution of this subspecies. The three birds wintered in
the same general area, suggesting a high level of connectivity between
breeding and wintering populations. Stutchbury et al. (2009) found a
similar connectivity for Wood Thrush (Hylocichla mustelina), not
previously documented for migratory songbirds. The large wintering areas
may reflect a temporal movement noted for each bird. The data indicate a
trend for each bird to be in the eastern portion of the kernels in
October with gradual movement west in April and May. The most likely
explanation for this replicated non-random change in position is that
the birds moved, perhaps following their food source. This net westward
directional movement is less likely to be an artifact due to shading or
weather-related variation because it was consistent among the three
birds tracked.

Northern Black Swift roost sites and roosting behavior in South
American wintering areas are unknown. Waterfalls, caves, and dripping
rock faces serve as roosting and breeding sites in breeding areas. There
is only one documented observation of a roost site for Northern Black
Swifts in South America, discovered during fall 1992 and 1993, on the
walls of a steep gorge along the Rio Cauca in the foothills of Colombia.
Black Swifts roosted consecutively at dusk for a week in a compact
group, mainly with White-collared Swifts (Streptoprocne zonaris),
clinging to the volcanic rock of a 40-m cliff overlooking the river,
indicating that rocky river banks are used as roosting sites during
migration (Stiles and Negret 1994). Similar sites may be used in
wintering areas if available, but this information is completely
lacking. Non-breeding Common Swifts (Apus apus) are known to
'roost' aerially in breeding areas and it is believed they
spend ~9 months of the year continuously on the wing. Non-breeding birds
may fly continuously for several years (Backman and Alerstam 2001,
Tarburton and Kaiser 2001). Common Swifts are also known to occasionally
roost at night by hanging on the foliage of trees (Holmgren 2004). Any
of these scenarios is possible for Northern Black Swifts in wintering
areas. Foraging activities of the Northern Black Swift in wintering
areas are unknown but kernel densities indicate the swifts range over a
large area in winter, suggesting the birds spend a lot of time on the
wing.

The capability of geolocators for tracking small birds is still
being explored and the potential is great. However, the devices are not
without limitations. A major obstacle for success is that once the
devices are deployed, the bird must be recaptured after a complete
migration cycle has occurred to obtain data. Our study indicates the
suitability of the Northern Black Swift for geolocator deployment and
recapture, primarily due to this species' strong nesting colony
fidelity and ability to carry small devices for long periods of time.

Calculation of latitude is unreliable around each equinox and near
the equator because length of day and night is equal. The accuracy of
calculated day length is especially affected for terrestrial species by
shading factors that alter recorded light levels such as cloudy weather,
foliage, and topographic shading of roost sites, resulting in latitude
uncertainties. Fudickar et al. (2011) found the devices had an error of
201 [+ or -] 43 km for latitude and 12 [+ or -] 3 km for longitude ([+
or -] 95% CI) for stationary geolocators (n = 30) in forested habitat.
The apparent retreat of bird #554 from Colorado to the Pacific Ocean
south of Baja California (Fig. 1) during spring migration is the result
of one data point and the accuracy of this fix is questionable. It may
or may not represent an actual movement by the bird and is possibly the
result of an extended period of shading. We did not eliminate this
position fix since the total day length did not drastically differ from
the other day lengths of that time period.

Accurate longitudinal information can be ascertained as this is not
affected by equinox and we successfully used longitude near the autumnal
equinox to indicate when the birds arrived at their wintering location.
Black Swift breeding requirements, such as nesting behind waterfalls in
deeply shaded niches in steep and narrow canyons, or in caves where the
performance of geolocators is often compromised by darkness, resulted in
some unusable data during the breeding season. Documented Black Swift
nocturnal roosting behavior during migration is limited and indicates
this could be a factor influencing the effectiveness of geolocators for
tracking this species. If winter nocturnal roost sites are similar to
those documented in migration and at breeding sites, this will also
influence the accuracy of the data collected by geolocators. Despite
these limitations, geolocators far surpass band recovery information or
dependence on sporadic sightings to identify migratory paths and winter
distribution of the Northern Black Swift.

Understanding the theory behind geolocation is extremely important
for interpreting and using the data collected to produce maps showing
animal movements (Hill 1994). Once the theory is understood, knowledge
of the behavior of the animal being studied and of weather patterns in
the area where the animal was tracked can be used to provide insight
into movement patterns. The mapped winter range of Black Swifts is an
area that typically experiences high cloud cover. Thus, a significant
number of the location fixes are most likely shifted to the north
artificially because of cloud cover in the winter range as compared to
the Colorado calibration location. Therefore, the southern portion of
the mapped winter range is most likely the area where the swifts spent
the winter. The technical limitations of geolocators and lack of
knowledge of Black Swift behavior in wintering areas, such as daily
foraging flight distance, and roosting locations and timing further
confound data interpretation.

The Black Swift is protected under the Migratory Bird Treaty Act in
the United States and the Convention for the Protection of Migratory
Birds and Game Mammals in Mexico. This study documents Northern Black
Swifts spending ~220 days in Brazil during winter 2009-2010, the first
records of the species in this country. This study identifies an annual
non-breeding geographic area of the Northern Black Swift and is a
significant step toward conservation of this species.

Future studies could include use of geolocators on subsets of
Northern Black Swifts from other areas of North America which would help
delineate the strength of migration connectivity for this subspecies.
Development of satellite transmitters small enough for use on Black
Swifts will provide greater accuracy than geolocators and can possibly
answer questions about roosting and foraging behavior.

CONSERVATION IMPLICATIONS

Knowledge of migratory pathways and winter distribution of a
species enables evaluation of those geographical areas, including
ecologic analysis and research, identification of potential habitat
threats, and development of conservation strategies. The homogeneity of
the wintering areas for Northern Black Swifts evidenced in this study
suggests limited winter resource use by this subspecies, which could
have long-term conservation impacts. The current rate of deforestation
in Brazil could directly threaten this subspecies. One of the most
refined computer models for simulating deforestation, SimAmazonia I,
indicates the rate of deforestation in the State of Amazonas will
increase rapidly in the coming decades which could result in a loss of
up to 30% of the forest cover by 2050 (Soares-Filho et al. 2006).
Climate change and global warming predictions also pose threats to
habitat and prey availability for this subspecies. Roberson and Collins
(2008) identified declines in some Northern Black Swift populations but
it is unknown if declines are due to environmental problems in breeding
areas, during migration, in wintering areas, or some combination of
these possibilities.

ACKNOWLEDGMENTS

The authors thank Black Canyon Audubon Society, Evergreen Audubon
Society, Grand Valley Audubon Society, Roaring Fork Audubon Society,
Colorado Field Ornithologists, and the Colorado Chapter of The Wildlife
Society for contributions to this project. D. M. Elwonger, H. E.
Kingery, L. R. Patrick, A. R. Robinsong, and W. P. Schmoker contributed
funds to the Richard G. Levad Memorial Fund held in trust at the Rocky
Mountain Bird Observatory to be used specifically for this project. The
Grand River Hospital perioperative staff contributed funds to the M. A.
Potter Memorial Fund to be used specifically for this project.
Significant assistance with interpretation of geolocator data was
received from N. B. F. Cousens and D. M. Morrison. A. O. Panjabi and L.
L. Jenks provided thoughtful reviews of the manuscript. N. M. Goedert,
T. W. Patrick, and C. W. Reichert contributed invaluable support during
Black Swift banding expeditions to Fulton Resurgence Cave. We thank the
White River National Forest for project support and logistics, K. H.
Knudsen for access to research library resources, and S. E. Hirshman for
coordinating access to Box Canyon Falls. Knowledgeable suggestions by
peer reviewers C. T. Collins and A. M. Fudickar were invaluable. This
publication is dedicated to the memory and spiritual guidance of our
friend and colleague Richard G. Levad.

Received 30 August 2011. Accepted 11 November 2011.

LITERATURE CITED

BACKMAN, J. AND Y. ALERSTAM. 2001. Confronting the winds:
orientation and flight behavior of roosting Swifts, Apus apus.
Proceedings of the Royal Society of London, Series B 268:1081-1087.